Tooth Resorption – Part 1: The evolvement, rationales and controversies of tooth resorption

Abstract In 1966, Andreasen and Hjørting‐Hansen were the first to describe a relationship between tooth resorption and dental trauma. However, Andreasen's original classification did not include other resorptive processes which have since been identified. Numerous articles have been published suggesting new terminology and definitions for tooth resorption. A uniform language with universally accepted terminology is crucial to eliminate the multiplicity of terms and definitions which only cause confusion within the profession. An electronic literature search was carried out in the PubMed database using the following keywords for articles published in English: “root resorption,” “inflammatory root resorption,” “replacement resorption,” “cervical resorption,” “trauma,” “ankylosis,” “surface resorption,” and “internal resorption.” The search also included textbooks and glossaries that may not have surfaced in the online search. This was done to identify articles related to tooth resorption and its etiology in dentistry. The aim of this review was to present the history that has led to the variety of terms and definitions for resorption. This review emphasizes the need for a clearer, simpler, and more comprehensive nomenclature for the various types of tooth resorption which are presented in Part 2 of this series.

responses of the tooth, PDL, and bone subsequent to trauma and a fourth response with no resorption. They named these responses as inflammatory resorption, replacement resorption, surface resorption, and healing with no resorption. Inflammatory resorption and replacement resorption were observed radiographically. 3 Later, in a histological evaluation of avulsed teeth, surface resorption was identified histologically but could not be detected radiographically. 4 Two other types of pathologic resorption were later added-first by Andreasen in 1975 5 and the second by Andreasen in 1986. 6 These were called transient replacement resorption and transient apical breakdown, respectively. 5,6 The latter is a condition where there is resorption of both bone and tooth substance as the root undergoes a remodeling process. It is no longer considered to be a pathological process but instead is considered to be part of a repair process that occurs in some cases. Hence, it will not be discussed further in this paper.
Inflammatory resorption (currently termed external inflammatory resorption) is radiographically characterized by the loss of tooth substance (cementum, dentin, and PDL) with an adjacent radiolucency in the bone. 7 It has been reported that inflammatory resorption can be arrested following adequate root canal treatment and later radiographic follow-up examination usually shows repair of the resorptive defects with re-establishment of normal PDL space. 7 In cases where endodontic treatment was not performed, the inflammatory resorption extended markedly, the teeth developed periapical radiolucencies indicating apical periodontitis as a result of the infected root canal system, and most often the outcome was loss of the tooth within the first year following trauma. 3 The term "inflammatory resorption" was adopted by most researchers and the American Association of Endodontists (AAE) in their glossary to describe not only teeth with this resorption after trauma but also teeth with apical resorption and a periapical radiolucency due to an infected root canal system. 1,8,9 Replacement resorption is the second type of response described by Andreasen and Hjørting-Hansen. 3,4 It is characterized by a pathologic loss of tooth substance (cementum, dentin, and PDL) with subsequent replacement of these tissues by bone, which results in fusion of the root to the surrounding bone. 1 This type of resorption occurs following severe trauma to teeth-such as intrusion, lateral luxation or avulsion-where the PDL and a large portion of the root surface have been damaged (typically, more than 20% of the root surface). 7 The initial process is known as ankylosis which is defined as loss of the PDL. 4 Ankylosis is effectively a fusion of the alveolar bone and dentin. It occurs when osteoclasts from the adjacent alveolar bone evolve at an early stage after the injury and adhere to the damaged root surface before the fibroblasts can reach the area to repair the PDL. 4,7 Once ankylosis occurs, replacement resorption will follow as tooth substance is resorbed by clastic cells and then it is replaced by bone. 4,7 Ankylosis is recognized radiographically by the lack of lamina dura and PDL (Figure 1), and clinically it is characterized by a metallic, higher pitched, or different sound when percussing the tooth. The term "replacement resorption" was also adopted by most researchers and the AAE in their Glossary. 1,10,11 Unlike inflammatory resorption, replacement resorption usually cannot be treated effectively, although occasionally it may be transient if only a small area of the root is involved. 5 Recently, Yoshpe et al. 12 presented a series of cases in which traumatized teeth developed ankylosis and regenerative endodontic treatment succeeded in arresting the advancement of the resorptive process and even reversed it. 12 However, more research is required to investigate this treatment in the case of ankylosis.
Surface resorption is a type of resorption of an inflammatory nature which is caused by an injury to the root surface. 3,4 The inflammation can be caused by mechanical stimuli (such as trauma or pressure) or by bacteria on the root surface. 3 If the stimulus is only present for a short period of time, healing may take place without the need for intervention. In most cases, the resorptive defects are F I G U R E 1 (A) Diagrammatic representation of ankylosis with external replacement resorption (reproduced with permission from Fuss et al. 21 ). (B) Radiographically, ankylosis is recognized by the lack of lamina dura and PDL while external replacement resorption is characterized by loos of tooth structure which is replaced by bone. This radiograph demonstrates a case of extensive ankylosis and replacement resorption of tooth 21

Transient internal inflammatory resorption Progressive external inflammatory resorption
Progressive external inflammatory resorption, orthodontic or endodontic problem. External inflammatory resorption may occur on the root apices of non-traumatized teeth with infected necrotic pulps A radiograph will reveal a periapical radiolucency associated with shortened root apices with a roughened root end Progressive external inflammatory resorption is subdivided into three groups: Cervical resorption Dento-alveolar ankylosis and replacement resorption Dento-alveolar ankylosis clinically, is recognized because of a lack of mobility of ankylosed teeth. These teeth will also have a special metallic percussion sound, and after some time they will be in infra-occlusion. Radiographically, dento-alveolar ankylosis may be recognized by the absence of a PDL space

Progressive internal resorption
Progressive internal resorption is the resorptive activity sustained by infection of necrotic pulp tissue in the root canal coronally to the area where the resorption takes place Trope 1998 9 (Review) Internal replacement resorption Histological appearance of the defects reveals the presence of metaplastic hard tissue replacing the resorbed dentine at the periphery of the defect, which is suggestive of active and simultaneous resorption and replacement.
This metaplastic hard tissue resembles cementum or osteoid-like tissues. However, detailed pathogenesis is not fully understood.
It has been suggested that IRR is an attempt of IIR to replace the damaged (resorbed) dentine. Diagnosis is made radiographically repaired with the formation of cementoid-like tissue. 13 If the affected area is larger and expands into the dentin, new cementum will follow, thus the contour of the root surface may only be partially restored. 3,4,8,13 This type of healing usually takes about 4 weeks to complete. 14,15 The type of the tissue that covers the resorbed root surface is dependent on the size of the area of root damage and the relative proximity of the cells to the damaged root surface. 4 It is also dependent on how far and how fast the cells travel in order to cover the damaged root surface. A localized injury over a small surface area favors cemental healing which is not detectable on radiographs (Table 1). 4 The complete healing of a tooth is characterized histologically by regeneration of the PDL with no radiographic signs of tooth or bone resorption. 3,4,6 In 1975, Andreasen reported the outcomes for 35 patients who had 40 permanent teeth avulsed and replanted. 5 In this report, a new condition, namely "transient replacement resorption," was used to describe teeth that initially had reduced mobility values which later returned to normal. Radiographic signs of transient replacement resorption were present in some cases. The teeth that exhibited transient replacement resorption had a significantly shorter extraoral dry period in comparison with teeth diagnosed with progressive replacement resorption. Later this type of response became known as surface resorption. 13 As outlined above, this type of resorption is an inflammatory process in response to a stimulus caused by damage to the root surface as a result of the injury. Without any further stimuli, this process will usually be self-limiting and healing will occur without any intervention. In most instances, the resorptive defects are repaired with the formation of cementoid-like tissue. 3,5 The definition of root resorption subsequent to dental trauma, described by Andreasen and Hjørting-Hansen, 3 various systemic diseases (for example, a cyst, ameloblastoma, giant cell tumor, fibro-osseous dysplasia) will lead to progressive inflammatory resorption (today, this resorption is termed either surface or pressure resorption). Removal of the stimuli in most cases will lead to cessation of the resorption and healing with a cementum-like tissue, and thus, it can be denoted as a transient resorptive process.
Without proper treatment, namely removing the stimuli, the resorption will continue and might lead to continued destruction of the tooth, which is known as progressive resorption. 8 Cervical resorption (known today as external cervical resorption, external invasive resorption, and various other names-see Tables 1 and 2) was described by Harrington  stimuli from bacteria originating in the gingival sulcus exist, the resorption will continue and will penetrate into the dentin but it will usually only affect the dental pulp in its later stages since the predentin protects the pulp from the resorbing cells. 8 When the resorption is long-standing, invading tissue may be seen undermining the enamel of the crown of the tooth, resulting in a pink appearance of the tooth. 22 However, to date, there is still great controversy among researchers and clinicians regarding the etiology, the nature of this type of resorption, and the terminology used. This type of resorption differs from inflammatory root resorption in that it frequently occurs in teeth with normal, healthy pulps and it is not associated with bacteria. Pulp involvement is rare and only occurs in severe or advanced cases. 23 Although the etiology remains vague, potential predisposing factors for this resorptive process include trauma, orthodontics, periodontal therapy, and internal bleaching. 24 Mavridou et al. 25 have reported that most of their external cervical resorption cases were observed in maxillary teeth (72%). The most frequent factor was orthodontics (45.7%) followed by trauma (28.5%), parafunctional habits (23.2%), poor oral health (22.9%), malocclusion (17.5%), and extraction of a neighboring tooth (14%). 25 The use of nano-CT, histology, and 3-dimensional imaging by Mavridou et al.
has significantly improved the understanding of the histopathology of this type of resorption. 26,27 Initially, surface resorption was considered to not be identifiable radiographically but only histologically. 2 In 1985, Andreasen named asymptomatic apical resorption following orthodontic treatment as "external surface resorption." 13 A number of terms have been used to identify the resorption of roots that has been induced by orthodontic tooth movement-such as "orthodontic tooth resorption" by Feiglin 16 and "transient inflammatory resorption" by Tronstad 8 (Table 2). In 1997, Bender et al. 28 Table 2).
The aim of this review was to present the history that has led to miscommunication between clinicians due to the variety of terms and definitions used for tooth resorption. These findings emphasize the need for clearer, simpler, and more comprehensive nomenclature for the various types of tooth resorption.

| ME THOD
An electronic literature search was carried out in the PubMed database using keywords listed in the Entree Terms database for articles published in English. The search employed a combined search strategy using the keywords "root resorption," "inflammatory root resorption," "replacement resorption," "cervical resorption," "trauma," "ankylosis," and "surface resorption." This was done to identify articles related to tooth resorption and its etiology in dentistry. The search also included textbooks and glossaries that may not have surfaced in the online search, which were manually identified along with relevant treatment recommendations for dentistry. Inclusion criteria included studies on humans and animals, as well as articles that included nomenclature in relation to trauma and dentistry.
All titles and abstracts were screened by the lead author (SL) for studies that met the eligibility criteria. Any questionable titles were discussed by all authors and the decision to include or exclude was made accordingly once consensus was reached. These titles were manually identified along with the relevant dental treatment recommendations. Exclusion criteria were studies that failed to meet the inclusion criteria, as well as conference proceedings, lectures, and letters to editors.

| RE VIE W
There are numerous classifications and terms for the same types of tooth resorption. For example, "apical replacement resorption" has been used for apical root resorption following orthodontic treatment. 28 The same pathological process has been included under the category of "inflammatory root resorption," 8 "superficial resorption," 13 "orthodontic-induced external root resorption," and "orthodontic tooth resorption." 22,36 This type of resorption has been named by the AAE as external surface resorption 1 and it includes resorption due to a tumor, an impacted tooth, etc.
The same problem exists for external cervical invasive resorption where at least 13 different terms have been used in various articles for this type of resorption-namely, "external resorption," "invasive cervical resorption," "root resorption due to periodontal infection," "external invasive resorption," "extra-canal invasive resorption," "odontoclastoma," "fibrous dysplasia of teeth," "burrowing resorption," "peripheral cervical resorption," "cervical external resorption," "supra-osseous extra-canal invasive resorption," "peripheral inflammatory root resorption," and "periodontal infection resorption." However, they all refer to the same condition. 1,7,17,24 There have been various attempts to classify tooth resorption according to etiology, 7 treatment, 16 the site of the resorption, 8,13,37,38 or the pathological process causing the inflammation and resorption. 8 When exploring resources of nomenclature in endodontics, such as the AAE Glossary of Endodontic Terms, 1 the general definition of resorption is based on the general anatomic origin of the resorption in the root-that is, external or internal. This definition is vague and unclear. Definitions of specific types of resorption are also very general and somewhat vague-for example, "surface resorption" is defined as "a physiologic process causing small superficial defects in the cementum and underlying dentin." This definition could include apical resorption due to orthodontic treatment or external apical resorption due to an adjacent pathologic process such as an ameloblastoma that can occur in teeth with normal, healthy pulps. 22 Hence, this definition is not specific enough to enable clinicians to distinguish between the different types of resorption.
The term "replacement resorption" can be problematic since whenever tooth substance is resorbed, it can be replaced by various types of tissue. Regardless of the etiology of the resorption, the replaced tissue could be bone, granulation tissue, cementum, or cementum-like tissues. Tronstad categorized this type of resorption under "inflammatory root resorption". 8 Replacement and inflammatory resorption are related to completely different etiologies, thus they require different terminology and different treatment protocols. 8,10 Similarly, inflammatory resorption is defined in the AAE Glossary the resorptive defect with external inflammatory resorption. The bone loss will appear as a radiolucency which is indicative of the space being occupied by the inflammatory response. This definition can include both an infected tooth with apical resorption, and teeth where the resorption is occurring anywhere along the length of the root following trauma (such as, avulsion or intrusion; Figure 2). The management of inflammatory resorption with lateral root and bone resorption following trauma is different to that for apical inflammatory resorption where there has been no previous trauma. 39,40 External inflammatory resorption can be divided into two sub-divisions according to the etiology and the location of the resorption as described by Trope 22 and Sak et al. 38 External apical inflammatory resorption is an infection-induced resorptive process which usually responds favorably to routine root canal treatment. 41 External lateral inflammatory resorption is correlated with severe luxation or avulsion injuries. The method of choice to treat a tooth with lateral inflammatory resorption has traditionally been to medicate the root canal system with long-term calcium hydroxide dressings until a continuous PDL space is observed radiographically along the root. 40,42,43 Recent studies on treatment with regenerative endodontics [44][45][46] and the use of corticosteroid-antibiotic compounds 39,40 as intracanal dressings have also been shown to be successful in arresting external lateral inflammatory resorption, and in much shorter time periods.
Endodontics is one part of the medical and dental professions that uses several terms and definitions to describe the same disease or condition. This problem exists not only in reference to tooth resorption, 47 but also in classifications of pulp, root canal, and periapical conditions. 40,43,48 This situation can lead to miscommunication between researchers, clinicians, and students resulting in a negative effect both on research and on clinical practice when treating patients. A clearer, simpler, and more comprehensive nomenclature needs to be developed for the various types of tooth resorption and this will be the subject of Part 2 of this series of articles.

| CON CLUS IONS
Tooth resorption is a complication that can lead to the loss of a tooth.
There are several types of tooth resorption with each having different etiology, pathogenesis, and management. There are many classifications and terms used to describe the same types of resorption which creates confusion amongst educators, researchers, authors, clinicians, and students. It can also lead to misconceptions which may eventually compromise the patient's treatment. Therefore, it is essential to develop a new clinically related and relevant classification of tooth resorption which will improve communication and provide clarity about each type of resorption.

CO N FLI C T O F I NTE R E S T
The authors declare that there are no conflicts of interest in this study.

AUTH O R CO NTR I B UTI O N
All authors contributed equally to the concept, design, literature searching, writing, revising and editing of this article.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing is not applicable to this article as no new data were created or analyzed in this study.